Trophoblast-derived CXCL12 promotes CD56


Journal

American journal of reproductive immunology (New York, N.Y. : 1989)
ISSN: 1600-0897
Titre abrégé: Am J Reprod Immunol
Pays: Denmark
ID NLM: 8912860

Informations de publication

Date de publication:
02 2020
Historique:
received: 17 07 2019
revised: 22 09 2019
accepted: 22 10 2019
pubmed: 28 10 2019
medline: 31 12 2020
entrez: 26 10 2019
Statut: ppublish

Résumé

Decidual natural killer (dNK) cells play key roles in maternal-fetal immune regulation, trophoblast invasion, and vascular remodeling, and most dNK cell populations are CD56 A total of 45 women with normal pregnancies and 8 unexplained recurrent spontaneous abortion (RSA) patients were included. We isolated primary human dNK (n = 53) and peripheral blood NK (pNK) cells (n = 5) from specimen and analyzed CD56, CD82, and CD29 by flow cytometry (FCM). We assessed their adhesion ability by cell counts of NK cells adhered to decidual stromal cells (DSCs) in a co-culture system. We found that RSA patients had more CD56 Trophoblast cells enhance the adhesive ability of NK cells to DSCs via the CXCL12/CD82/CD29 signaling pathway and contribute to CD56

Identifiants

pubmed: 31650642
doi: 10.1111/aji.13203
doi:

Substances chimiques

CD56 Antigen 0
CD82 protein, human 0
CXCL12 protein, human 0
Chemokine CXCL12 0
Integrin beta1 0
Itgb1 protein, human 0
Kangai-1 Protein 0
NCAM1 protein, human 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National Basic Research Program of China
ID : 2015CB943300
Pays : International
Organisme : National Key Research and Development Program of China
ID : 2017YFC1001404
Pays : International
Organisme : National Natural Science Foundation of China
ID : 31671200
Pays : International
Organisme : National Natural Science Foundation of China
ID : 31970798
Pays : International
Organisme : National Natural Science Foundation of China
ID : 81490744
Pays : International
Organisme : National Natural Science Foundation of China
ID : 81671460
Pays : International
Organisme : National Natural Science Foundation of China
ID : 81730039
Pays : International
Organisme : Shanghai Rising-Star Program
ID : 16QA1400800
Pays : International
Organisme : Innovation-oriented Science and Technology Grant from NPFPC Key Laboratory of Reproduction Regulation
ID : CX2017-2
Pays : International
Organisme : Shanghai Municipal Medical and Health Discipline Construction Projects
ID : 2017ZZ02015
Pays : International

Informations de copyright

© 2019 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.

Références

Hanna J, Goldman-Wohl D, Hamani Y, et al. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med. 2006;12:1065-1074.
Robson A, Harris LK, Innes BA, et al. Uterine natural killer cells initiate spiral artery remodeling in human pregnancy. FASEB J. 2012;26:4876-4885.
Vacca P, Moretta L, Moretta A, Mingari MC. Origin, phenotype and function of human natural killer cells in pregnancy. Trends Immunol. 2011;32:517-523.
Cerdeira AS, Rajakumar A, Royle CM, et al. Conversion of peripheral blood NK cells to a decidual NK-like phenotype by a cocktail of defined factors. J Immunol. 2013;190:3939-3948.
Hanna J, Wald O, Goldman-Wohl D, et al. CXCL12 expression by invasive trophoblasts induces the specific migration of CD16- human natural killer cells. Blood. 2003;102:1569-1577.
Wu X, Jin LP, Yuan MM, Zhu Y, Wang MY, Li DJ. Human first-trimester trophoblast cells recruit CD56brightCD16- NK cells into decidua by way of expressing and secreting of CXCL12/stromal cell-derived factor 1. J Immunol. 2005;175:61-68.
Piao HL, Wang SC, Tao Y, Fu Q, Du MR, Li DJ. CXCL12/CXCR4 signal involved in the regulation of trophoblasts on peripheral NK cells leading to Th2 bias at the maternal-fetal interface. Eur Rev Med Pharmacol Sci. 2015;19:2153-2161.
Vacca P, Vitale C, Montaldo E, et al. CD34+ hematopoietic precursors are present in human decidua and differentiate into natural killer cells upon interaction with stromal cells. Proc Natl Acad Sci USA. 2011;108:2402-2407.
Keskin DB, Allan DS, Rybalov B, et al. TGFbeta promotes conversion of CD16+ peripheral blood NK cells into CD16- NK cells with similarities to decidual NK cells. Proc Natl Acad Sci USA. 2007;104:3378-3383.
Su Y, Lei X, Wu L, Liu L. The role of endothelial cell adhesion molecules P-selectin, E-selectin and intercellular adhesion molecule-1 in leucocyte recruitment induced by exogenous methylglyoxal. Immunology. 2012;137:65-79.
Petri B, Phillipson M, Kubes P. The physiology of leukocyte recruitment: An in vivo perspective. J Immunol. 2008;180:6439-6446.
Elangbam CS, Qualls CW Jr, Dahlgren RR. Cell adhesion molecules-update. Vet Pathol. 1997;34:61-73.
Ehirchiou D, Muller YD, Chicheportiche R, et al. Chemoattractant signals and adhesion molecules promoting human regulatory T cell recruitment to porcine endothelium. Transplantation. 2016;100:753-762.
Fan X, Rudensky AY. Hallmarks of tissue-resident lymphocytes. Cell. 2016;164:1198-1211.
Montaldo E, Vacca P, Chiossone L, et al. Unique Eomes(+) NK cell subsets are present in uterus and decidua during early pregnancy. Front Immunol. 2015;6:646.
Yurdakan G, Ekem TE, Bahadir B, Gun BD, Kuzey GM, Ozdamar SO. Expression of adhesion molecules in first trimester spontaneous abortions and their role in abortion pathogenesis. Acta Obstet Gynecol Scand. 2008;87:775-782.
Szarka A, Rigo J Jr, Lazar L, Beko G, Molvarec A. Circulating cytokines, chemokines and adhesion molecules in normal pregnancy and preeclampsia determined by multiplex suspension array. BMC Immunol. 2010;11:59.
Liu Q, Zhang B, Zhao X, Zhang Y, Liu Y, Yan X. Blockade of adhesion molecule CD146 causes pregnancy failure in mice. J Cell Physiol. 2008;215:621-626.
Liu WM, Zhang XA. KAI1/CD82, a tumor metastasis suppressor. Cancer Lett. 2006;240:183-194.
Yang X, Wei LL, Tang C, Slack R, Mueller S, Lippman ME. Overexpression of KAI1 suppresses in vitro invasiveness and in vivo metastasis in breast cancer cells. Cancer Res. 2001;61:5284-5288.
Jee B, Jin K, Hahn JH, Song HG, Lee H. Metastasis-suppressor KAI1/CD82 induces homotypic aggregation of human prostate cancer cells through Src-dependent pathway. Exp Mol Med. 2003;35:30-37.
Abe M, Sugiura T, Takahashi M, Ishii K, Shimoda M, Shirasuna K. A novel function of CD82/KAI-1 on E-cadherin-mediated homophilic cellular adhesion of cancer cells. Cancer Lett. 2008;266:163-170.
Lee MS, Byun HJ, Lee J, Jeoung DI, Kim YM, Lee H. Tetraspanin CD82 represses Sp1-mediated Snail expression and the resultant E-cadherin expression interrupts nuclear signaling of beta-catenin by increasing its membrane localization. Cell Signal. 2018;52:83-94.
Berditchevski F, Odintsova E. Characterization of integrin-tetraspanin adhesion complexes: role of tetraspanins in integrin signaling. J Cell Biol. 1999;146:477-492.
Mannion BA, Berditchevski F, Kraeft SK, Chen LB, Hemler ME. Transmembrane-4 superfamily proteins CD81 (TAPA-1), CD82, CD63, and CD53 specifically associated with integrin alpha 4 beta 1 (CD49d/CD29). J Immunol. 1996;157:2039-2047.
Sridhar SC, Miranti CK. Tetraspanin KAI1/CD82 suppresses invasion by inhibiting integrin-dependent crosstalk with c-Met receptor and Src kinases. Oncogene. 2006;25:2367-2378.
Lee JH, Seo YW, Park SR, Kim YJ, Kim KK. Expression of a splice variant of KAI1, a tumor metastasis suppressor gene, influences tumor invasion and progression. Cancer Res. 2003;63:7247-7255.
Lee HA, Park I, Byun HJ, Jeoung D, Kim YM, Lee H. Metastasis suppressor KAI1/CD82 attenuates the matrix adhesion of human prostate cancer cells by suppressing fibronectin expression and beta1 integrin activation. Cell Physiol Biochem. 2011;27:575-586.
Abram CL, Lowell CA. The ins and outs of leukocyte integrin signaling. Annu Rev Immunol. 2009;27:339-362.
Wang S, Zhou X, Yang J. Integrin alphavbeta3 is essential for maintenance of decidua tissue homeostasis and of natural killer cell immune tolerance during pregnancy. Reprod Sci. 2018;25:1424-1430.
Gellersen B, Briese J, Oberndorfer M, et al. Expression of the metastasis suppressor KAI1 in decidual cells at the human maternal-fetal interface: Regulation and functional implications. Am J Pathol. 2007;170:126-139.
Zhang Q, Tan D, Luo W, Lu J, Tan Y. Expression of CD82 in human trophoblast and its role in trophoblast invasion. PLoS ONE. 2012;7:e38487.
Li MQ, Hou XF, Shao J, Tang CL, Li DJ. The DSCs-expressed CD82 controls the invasiveness of trophoblast cells via integrin beta1/MAPK/MAPK3/1 signaling pathway in human first-trimester pregnancy. Biol Reprod. 2010;82:968-979.
Shibagaki N, Hanada K, Yamashita H, Shimada S, Hamada H. Overexpression of CD82 on human T cells enhances LFA-1 / ICAM-1-mediated cell-cell adhesion: functional association between CD82 and LFA-1 in T cell activation. Eur J Immunol. 1999;29:4081-4091.
Delaguillaumie A, Harriague J, Kohanna S, et al. Tetraspanin CD82 controls the association of cholesterol-dependent microdomains with the actin cytoskeleton in T lymphocytes: relevance to co-stimulation. J Cell Sci. 2004;117:5269-5282.
Delaguillaumie A, Lagaudriere-Gesbert C, Popoff MR, Conjeaud H. Rho GTPases link cytoskeletal rearrangements and activation processes induced via the tetraspanin CD82 in T lymphocytes. J Cell Sci. 2002;115:433-443.
Yeung L, Hickey MJ, Wright MD. The many and varied roles of tetraspanins in immune cell recruitment and migration. Front Immunol. 2018;9:1644.
Meng YH, Zhou WJ, Jin LP, et al. RANKL-mediated harmonious dialogue between fetus and mother guarantees smooth gestation by inducing decidual M2 macrophage polarization. Cell Death Dis. 2017;8:e3105.
Li YH, Zhou WH, Tao Y, et al. The Galectin-9/Tim-3 pathway is involved in the regulation of NK cell function at the maternal-fetal interface in early pregnancy. Cell Mol Immunol. 2016;13:73-81.
Wang XQ, Zhou WJ, Hou XX, Fu Q, Li DJ. Trophoblast-derived CXCL16 induces M2 macrophage polarization that in turn inactivates NK cells at the maternal-fetal interface. Cell Mol Immunol. 2018;15:1038-1046.
Fu B, Wei H. Decidual natural killer cells and the immune microenvironment at the maternal-fetal interface. Sci China Life Sci. 2016;59:1224-1231.
Vacca P, Cantoni C, Vitale M, et al. Crosstalk between decidual NK and CD14+ myelomonocytic cells results in induction of Tregs and immunosuppression. Proc Natl Acad Sci USA. 2010;107:11918-11923.
Guimond M-J, Wang B, Croy BA. Engraftment of Bone Marrow from Severe Combined Immunodeficient (SCID) mice reverses the reproductive deficits in natural killer cell-deficient tgε26 mice. J Exp Med. 1998;187:217-223.
Herington JL, Bany BM. The conceptus increases secreted phosphoprotein 1 gene expression in the mouse uterus during the progression of decidualization mainly due to its effects on uterine natural killer cells. Reproduction. 2007;133:1213-1221.
Dambaeva SV, Durning M, Rozner AE, Golos TG. Immunophenotype and cytokine profiles of rhesus monkey CD56bright and CD56dim decidual natural killer cells. Biol Reprod. 2012;86:1-10.
El Costa H, Casemayou A, Aguerre-Girr M, et al. Critical and differential roles of NKp46- and NKp30-activating receptors expressed by uterine NK cells in early pregnancy. J Immunol. 2008;181:3009-3017.
Grier JT, Forbes LR, Monaco-Shawver L, et al. Human immunodeficiency-causing mutation defines CD16 in spontaneous NK cell cytotoxicity. J Clin Invest. 2012;122:3769-3780.
Marlin R, Duriez M, Berkane N, et al. Dynamic shift from CD85j/ILT-2 to NKG2D NK receptor expression pattern on human decidual NK during the first trimester of pregnancy. PLoS ONE. 2012;7:e30017.
Frey M, Packianathan NB, Fehniger TA, et al. Differential expression and function of L-selectin on CD56bright and CD56dim natural killer cell subsets. J Immunol. 1998;161:400-408.
Chantakru S, Miller C, Roach LE, et al. Contributions from self-renewal and trafficking to the uterine NK cell population of early pregnancy. J Immunol. 2002;168:22-28.
Yamamoto T, Takahashi Y, Kase N, Mori H. Decidual natural killer cells in recurrent spontaneous abortion with normal chromosomal content. Am J Reprod Immunol. 1999;41:337-342.
Gao Y, Wang PL. Increased CD56(+) NK cells and enhanced Th1 responses in human unexplained recurrent spontaneous abortion. Genet Mol Res. 2015;14:18103-18109.
Nakashima A, Shiozaki A, Myojo S, et al. Granulysin produced by uterine natural killer cells induces apoptosis of extravillous trophoblasts in spontaneous abortion. Am J Pathol. 2008;173:653-664.
Zhang Y, Zhao A, Wang X, Shi G, Jin H, Lin Q. Expressions of natural cytotoxicity receptors and NKG2D on decidual natural killer cells in patients having spontaneous abortions. Fertil Steril. 2008;90:1931-1937.
Piao HL, Tao Y, Zhu R, et al. The CXCL12/CXCR4 axis is involved in the maintenance of Th2 bias at the maternal/fetal interface in early human pregnancy. Cell Mol Immunol. 2012;9:423-430.
Ordi J, Casals G, Ferrer B, et al. Uterine (CD56+) natural killer cells recruitment: association with decidual reaction rather than embryo implantation. Am J Reprod Immunol. 2006;55:369-377.
Diedrich K, Fauser BC, Devroey P, Griesinger G, Evian Annual Reproduction Workshop G. The role of the endometrium and embryo in human implantation. Hum Reprod Update. 2007;13:365-377.
Feng Y, Ma X, Deng L, et al. Role of selectins and their ligands in human implantation stage. Glycobiology. 2017;27:385-391.
King A, Loke YW. Differential expression of blood-group-related carbohydrate antigens by trophoblast subpopulations. Placenta. 1988;9:513-521.
James JL, Cartwright JE, Whitley GS, Greenhill DR, Hoppe A. The regulation of trophoblast migration across endothelial cells by low shear stress: consequences for vascular remodelling in pregnancy. Cardiovasc Res. 2012;93:152-161.
Fernekorn U, Butcher EC, Behrends J, Hartz S, Kruse A. Functional involvement of P-selectin and MAdCAM-1 in the recruitment of alpha4beta7-integrin-expressing monocyte-like cells to the pregnant mouse uterus. Eur J Immunol. 2004;34:3423-3433.
Zenclussen AC, Fest S, Sehmsdorf US, Hagen E, Klapp BF, Arck PC. Upregulation of decidual P-selectin expression is associated with an increased number of Th1 cell populations in patients suffering from spontaneous abortions. Cell Immunol. 2001;213:94-103.
Kim C, Ye F, Ginsberg MH. Regulation of integrin activation. Annu Rev Cell Dev Biol. 2011;27:321-345.
Nardo LG, Nikas G, Makrigiannakis A, Sinatra F, Nardo F. Synchronous expression of pinopodes and alpha v beta 3 and alpha 4 beta 1 integrins in the endometrial surface epithelium of normally menstruating women during the implantation window. J Reprod Med. 2003;48:355-361.
Lessey BA, Castelbaum AJ, Buck CA, Lei Y, Yowell CW, Sun J. Further characterization of endometrial integrins during the menstrual cycle and in pregnancy. Fertil Steril. 1994;62:497-506.
Staun-Ram E, Shalev E. Human trophoblast function during the implantation process. Reprod Biol Endocrinol. 2005;3:56.
Kabir-Salmani M, Shiokawa S, Akimoto Y, et al. Alphavbeta3 integrin signaling pathway is involved in insulin-like growth factor I-stimulated human extravillous trophoblast cell migration. Endocrinology. 2003;144:1620-1630.
Ruck P, Marzusch K, Kaiserling E, et al. Distribution of cell adhesion molecules in decidua of early human pregnancy. An immunohistochemical study. Lab Invest. 1994;71:94-101.
Kabir-Salmani M, Shiokawa S, Akimoto Y, Sakai K, Iwashita M. The role of alpha(5)beta(1)-integrin in the IGF-I-induced migration of extravillous trophoblast cells during the process of implantation. Mol Hum Reprod. 2004;10:91-97.
Stephens LE, Sutherland AE, Klimanskaya IV, et al. Deletion of beta 1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes Dev. 1995;9:1883-1895.
Zhang J, Dunk CE, Kwan M, et al. Human dNK cell function is differentially regulated by extrinsic cellular engagement and intrinsic activating receptors in first and second trimester pregnancy. Cell Mol Immunol. 2017;14:203-213.
Miranti CK, Brugge JS. Sensing the environment: a historical perspective on integrin signal transduction. Nat Cell Biol. 2002;4:E83-90.

Auteurs

Han Lu (H)

NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China.
Institute of Obstetrics and Gynecology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China.

Li-Ping Jin (LP)

Clinical and Translational Research Center, Shanghai First Maternity and Infant Hospital, Tongji University School of Medicine, Shanghai, China.

Hong-Lan Huang (HL)

Institute of Obstetrics and Gynecology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China.

Si-Yao Ha (SY)

Institute of Obstetrics and Gynecology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China.

Hui-Li Yang (HL)

Institute of Obstetrics and Gynecology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China.

Rui-Qi Chang (RQ)

Institute of Obstetrics and Gynecology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China.

Da-Jin Li (DJ)

NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China.
Institute of Obstetrics and Gynecology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China.

Ming-Qing Li (MQ)

NHC Key Lab of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China.
Institute of Obstetrics and Gynecology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China.
Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH